Histochemistry and Cell Biology

, Volume 130, Issue 4, pp 709–717 | Cite as

Heterotypic tubular connections at the endoplasmic reticulum–Golgi complex interface

  • Guillermo Vivero-Salmerón
  • José Ballesta
  • José A. Martínez-Menárguez
Original Paper


Electron microscopy and cryoimmunocytochemistry were used to characterize tubular connections in the secretory pathway using rat spermatids as model. Our results support the existence of a complex tubular network enriched in the Golgi matrix protein GM130 that transiently joins the cis-Golgi side and the endoplasmic reticulum. These tubules occasionally contain the endoplasmic reticulum resident protein PDI but not COPII complexes or KDEL receptor. At the lateral edges of the stacks tubules were seen to connect cisternae belonging to the same or adjacent stacks. These connections were observed in all cisternae but preferentially on the cis side. Giantin, Gos28 and Rab6 were detected in the tubules; importantly, we reported the presence of cistrans heterotypic connections between cisternae. On the trans-Golgi side, we occasionally observed tubules highly immunoreactive for Rab6 connecting the stack with the forming acrosome. Together, our results support the existence of transient continuities throughout the secretory pathways.


Golgi complex Spermatid Tubule Electron microscopy Cryoimmunocytochemistry 



cis-Golgi network


Endoplasmic reticulum


Endoplasmic reticulum–Golgi intermediate compartment


Protein disulfide isomerase


trans-Golgi network


  1. Bannykh SI, Balch WE (1997) Membrane dynamics at the endoplasmic reticulum–Golgi interface. J Cell Biol 138:1–4PubMedCrossRefGoogle Scholar
  2. Ben-Tekaya H, Miura K, Pepperkok R, Hauri HP (2005) Live imaging of bidirectional traffic from the ERGIC. J Cell Sci 118:357–367PubMedCrossRefGoogle Scholar
  3. Bonifacino J, Glick BS (2004) The mechanisms of vesicle budding and fusion. Cell 116:153–166PubMedCrossRefGoogle Scholar
  4. Chen X, Walker AK, Strahler JR, Simon ES, Tomanicek-Volk SL, Nelson BB, Hurley MC, Ernst SA, Williams JA, Andrews PC (2006) Organellar proteomics: analysis of pancreatic zymogen granule membranes. Mol Cell Proteomics 5:306–312PubMedGoogle Scholar
  5. Clermont Y, Rambourg A, Hermo L (1994) Connections between the various elements of the cis- and mid-compartments of the Golgi apparatus of early rat spermatids. Anat Rec 240:469–480PubMedCrossRefGoogle Scholar
  6. Darchen F, Goud B (2000) Multiple aspects of Rab protein action in the secretory pathway: focus on Rab3 and Rab6. Biochimie 82:375–384PubMedCrossRefGoogle Scholar
  7. Glick BS (2000) Organization of the Golgi apparatus. Curr Opin Cell Biol 12:450–456PubMedCrossRefGoogle Scholar
  8. Griffiths G (2000) Gut thoughts on the Golgi complex. Traffic 1:738–745PubMedCrossRefGoogle Scholar
  9. Hermo L, Rambourg A, Clermont Y (1980) Three dimensional architecture of the cortical region of the Golgi apparatus in rat spermatids. Am J Anat 157:357–373PubMedCrossRefGoogle Scholar
  10. Klumperman J (2000) Transport between ER and Golgi. Curr Opin Cell Biol 12:445–449PubMedCrossRefGoogle Scholar
  11. Klumperman J, Schweizer A, Clausen H, Tang BL, Hong W, Oorschot V, Hauri H-P (1998) The recycling pathway of protein ERGIC-53 and dynamics of the ER-Golgi intermediate compartment. J Cell Sci 111:3411–3425PubMedGoogle Scholar
  12. Ladinsky MS, Kremer JR, Furcinitti PS, McIntosh JR, Howell KE (1994) HVEM tomography of the trans-Golgi network: structural insights and identification of a lace-like vesicle coat. J Cell Biol 127:29–38PubMedCrossRefGoogle Scholar
  13. Ladinsky MS, Mastronarde DN, McIntosh JR, Howell KE, Staehelin LA (1999) Golgi structure in three dimensions: functional insights from the normal rat kidney cell. J Cell Biol 144:1135–1149PubMedCrossRefGoogle Scholar
  14. Lippincott-Schwartz J, Roberts TH, Hirschberg K (2000) Secretory protein trafficking and organelle dynamics in living cells. Annu Rev Cell Dev Biol 16:557–589PubMedCrossRefGoogle Scholar
  15. Marra P, Salvatore L, Mironov A Jr, Di Campli A, Di Tullio G, Trucco A, Beznoussenko G, Mironov A, De Matteis MA (2007) The biogenesis of the Golgi ribbon: the roles of membrane input from the ER and of GM130. Mol Biol Cell 18:1595–1608PubMedCrossRefGoogle Scholar
  16. Marsh BJ, Volkmann N, McIntosh JR, Howell KE (2004) Direct continuities between cisternae at different levels of the Golgi complex in glucose-stimulated mouse islet beta cells. Proc Natl Acad Sci USA 101:5565–5570PubMedCrossRefGoogle Scholar
  17. Martínez-Alonso E, Egea G, Ballesta J, Martínez-Menárguez JA (2005) Structure and dynamics of the Golgi complex at 15 degrees C: low temperature induces the formation of Golgi-derived tubules. Traffic 6:32–44PubMedCrossRefGoogle Scholar
  18. Martínez-Alonso E, Ballesta J, Martínez-Menárguez JA (2007) Low-temperature-induced Golgi tubules are transient membranes enriched in molecules regulating intra-Golgi transport. Traffic 8:359–368PubMedCrossRefGoogle Scholar
  19. Martínez-Menárguez JA, Geuze HJ, Ballesta J (1996a) Identification of two types of beta-COP vesicles in the Golgi complex of rat spermatids. Eur J Cell Biol 71:137–143PubMedGoogle Scholar
  20. Martínez-Menárguez JA, Geuze HJ, Ballesta J (1996b) Evidence for a nonlysosomal origin of the acrosome. J Histochem Cytochem 44:313–320PubMedGoogle Scholar
  21. Martínez-Menárguez JA, Geuze HJ, Slot JW, Klumperman J (1999) Vesicular tubular clusters between the ER and Golgi mediate concentration of soluble secretory protein by exclusion from COPI-coated vesicles. Cell 98:81–90PubMedCrossRefGoogle Scholar
  22. Martinez-Menarguez JA, Prekeris R, Oorschot VM, Scheller R, Slot JW, Geuze HJ, Klumperman J (2001) Peri-Golgi vesicles contain retrograde but not anterograde proteins consistent with the cisternal progression model of intra-Golgi transport. J Cell Biol 155:1213–1224PubMedCrossRefGoogle Scholar
  23. Matsuura-Tokita K, Takeuchi M, Ichihara A, Mikuriya K, Nakano A (2006) Live imaging of yeast Golgi cisternal maturation. Nature 441:1007–1010PubMedCrossRefGoogle Scholar
  24. Mironov AA, Weidman P, Luini A (1997) Variations on the intracellular transport theme:maturing cisternae and trafficking tubules. J Cell Biol 138:481–484PubMedCrossRefGoogle Scholar
  25. Mollenhauer HH, Morré DJ (1998) The tubular network of the Golgi apparatus. Histochem Cell Biol 109:533–543PubMedCrossRefGoogle Scholar
  26. Orci L, Stamnes M, Ravazzola M, Amherdt M, Perrelet A, Söllner TH, Rothman JE (1997) Bidirectional transport by distinct populations of COPI-coated vesicles. Cell 90:335–349PubMedCrossRefGoogle Scholar
  27. Patterson GH, Hirschberg K, Polishchuk RS, Gerlich D, Phair RD, Lippincott-Schwartz J (2008) Transport through the Golgi apparatus by rapid partitioning within a two-phase membrane system. Cell 133:1055–1067PubMedCrossRefGoogle Scholar
  28. Polishchuk RS, Mironov AA (2004) Structural aspects of Golgi function. Cell Mol Life Sci 61:146–158PubMedCrossRefGoogle Scholar
  29. Polishchuk RS, Polishchuk EV, Marra P, Alberti S, Buccione R, Luini A, Mironov AA (2000) Correlative light-electron microscopy reveals the tubular-saccular ultrastructure of carriers operating between Golgi apparatus and plasma membrane. J Cell Biol 148:45–58PubMedCrossRefGoogle Scholar
  30. Rambourg A, Clermont Y (1990) Three-dimensional electron microscopy: structure of the Golgi apparatus. Eur J Cell Biol 51:189–200PubMedGoogle Scholar
  31. Sciaky N, Presley J, Smith C, Zaal KJ, Cole N, Moreira JE, Terasaki M, Siggia E, Lippincott-Schwartz J (1997) Golgi tubule traffic and the effects of brefeldin A visualized in living cells. J Cell Biol 139:1137–1155PubMedCrossRefGoogle Scholar
  32. Short B, Haas A, Barr FA (2005) Golgins and GTPases, giving identity and structure to the Golgi apparatus. Biochim Biophys Acta 1744:383–395PubMedCrossRefGoogle Scholar
  33. Simpson JC, Nilsson T, Pepperkok R (2006) Biogenesis of tubular ER-to-Golgi transport intermediates. Mol Biol Cell 17:723–737PubMedCrossRefGoogle Scholar
  34. Thorne-Tjömsland G, Dumontier M, Jamieson JC (1998) 3D topography of noncompact zone Golgi tubules in rat spermatids: a computer-assisted serial section reconstruction study. Anat Rec 250:381–396PubMedCrossRefGoogle Scholar
  35. Trucco A, Polishchuk RS, Martella O, Di Pentima A, Fusella A, Di Giandomenico D, San Pietro E, Beznoussenko GV, Polishchuk EV, Baldassarre M, Buccione R, Geerts WJ, Koster AJ, Burger KN, Mironov AA, Luini A (2004) Secretory traffic triggers the formation of tubular continuities across Golgi sub-compartments. Nat Cell Biol 6:1071–1081PubMedCrossRefGoogle Scholar
  36. Zeuschner D, Geerts WJ, van Donselaar E, Humbel BM, Slot JW, Koster AJ, Klumperman J (2006) Immuno-electron tomography of ER exit sites reveals the existence of free COPII-coated transport carriers. Nat Cell Biol 8:377–383PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Guillermo Vivero-Salmerón
    • 1
  • José Ballesta
    • 1
  • José A. Martínez-Menárguez
    • 1
  1. 1.Department of Cell Biology and Histology, School of MedicineUniversity of MurciaMurciaSpain

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